What Does Not Kill Them, Makes Them Stronger: Is the Inappropriate Use of Biocides a Driver of Antimicrobial Resistance?

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Bacterial Pathogens".

Deadline for manuscript submissions: closed (15 December 2023) | Viewed by 18136

Special Issue Editors


E-Mail Website1 Website2
Guest Editor
Department of Biological Safety, German Federal Institute for Risk Assessment, 10589 Berlin, Germany
Interests: antimicrobial resistance

E-Mail Website1 Website2
Guest Editor
Department of Biological Safety, German Federal Institute for Risk Assessment, 10589 Berlin, Germany
Interests: antimicrobial resistance

Special Issue Information

Dear colleagues,

Biocides are used worldwide as components of numerous consumer products, antiseptics and disinfectants. They are applied in various settings, such as stables, food production facilities, private households and hospitals, where they help to prevent the transmission of microbial pathogens and consequently reduce the risk of infection. The improper use of biocides, however, can exert selective stress to microorganisms including pathogens. Concerns have been raised about the unintended release of sublethal concentrations of biocides and their impact on bacteria including the development of cross- and co-resistance to biocides and antibiotics. To tackle potential undesired effects of biocides an interdisciplinary approach is indispensable. However, One Health currently focus primarily on the reduction of antibiotic usage.

This special issue offers an open-access forum that aims to present novel knowledge of any viewpoint related to the impacts of biocides on microorganisms including epidemiological and mechanistic studies, description of innovative experimental techniques and regulatory aspects. Studies may focus on the microbial stress response and adaptation to biocides, inherent and acquired resistance mechanisms, the role of horizontal transfer of mobile genetic elements and mutations, the biocidal impact on microbial communities and the role of biofilms as well as the influence of biocides on microbial pathogenicity and persistence. High-quality original articles, reviews, and commentaries are welcome.

Prof. Dr. Sascha Al Dahouk
Dr. Ralf Dieckmann
Guest Editors

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Keywords

  • biocides
  • antibiotics
  • resistance
  • hygiene
  • stress response
  • adaptation
  • microbiology
  • persistence
  • pathogenicity
  • antimicrobial
  • tolerance
  • biofilm
  • disinfection
  • preservation
  • antisepsis

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Published Papers (5 papers)

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Research

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17 pages, 294 KiB  
Article
Development of Quality Control Ranges for Biocide Susceptibility Testing
by Angela R. Schug, Anissa D. Scholtzek, John Turnidge, Marita Meurer, Stefan Schwarz, Andrea T. Feßler and the Biocide Susceptibility Study Group
Pathogens 2022, 11(2), 223; https://doi.org/10.3390/pathogens11020223 - 8 Feb 2022
Cited by 4 | Viewed by 2159
Abstract
Every laboratory test needs validation by quality controls. For biocide susceptibility testing (BST), neither quality control (QC) strains nor QC ranges applicable to these strains are currently available. As QC strains, four well-defined laboratory reference strains (Staphylococcus aureus ATCC® 6538, Enterococcus [...] Read more.
Every laboratory test needs validation by quality controls. For biocide susceptibility testing (BST), neither quality control (QC) strains nor QC ranges applicable to these strains are currently available. As QC strains, four well-defined laboratory reference strains (Staphylococcus aureus ATCC® 6538, Enterococcus hirae ATCC® 10541, Escherichia coli ATCC® 10536 and Pseudomonas aeruginosa ATCC® 15442), which have been used previously for biocide efficacy testing, were selected. In an interlaboratory trial with eleven participating laboratories, BST QC ranges should be developed for the aforementioned four strains and the four biocides benzalkonium chloride, chlorhexidine, octenidine and polyhexanide. The performance of three different lots of tryptic soy broth was explored using the broth microdilution method and the data were subsequently evaluated using the RangeFinder software. As a result, QC ranges were defined for all reference strain–biocide combinations, except for P. aeruginosa ATCC® 15442 with the two biocides chlorhexidine and polyhexanide. The development of the latter two QC ranges was not possible, due to the limited solubility of the biocides in the test range required for P. aeruginosa ATCC® 15442. The newly developed QC ranges comprise three to five dilution steps. The establishment of QC ranges will contribute to the validation of BST in the future. Full article
11 pages, 1134 KiB  
Article
Exposure to Quaternary Ammonium Compounds Selects Resistance to Ciprofloxacin in Listeria monocytogenes
by Alizée Guérin, Arnaud Bridier, Patricia Le Grandois, Yann Sévellec, Federica Palma, Benjamin Félix, LISTADAPT Study Group, Sophie Roussel and Christophe Soumet
Pathogens 2021, 10(2), 220; https://doi.org/10.3390/pathogens10020220 - 18 Feb 2021
Cited by 28 | Viewed by 3815
Abstract
In this contribution, the antimicrobial susceptibility toward 11 antibiotics and four biocides of a panel of 205 Listeria monocytogenes (Lm) strains isolated from different ecological niches (i.e., food, animals and natural environment) was evaluated. The impact of exposure to biocides on the antibiotic [...] Read more.
In this contribution, the antimicrobial susceptibility toward 11 antibiotics and four biocides of a panel of 205 Listeria monocytogenes (Lm) strains isolated from different ecological niches (i.e., food, animals and natural environment) was evaluated. The impact of exposure to biocides on the antibiotic susceptibilities of Lm was also investigated. Lm strains isolated from food exhibited overall a lower susceptibility (higher minimal inhibitory concentrations, MIC) for ammonium quaternary compounds (QACs) and peracetic acid (PAC) than strains isolated from animals and natural environments. Conversely, the ecological origins of Lm strains did not significantly affect their susceptibilities towards antibiotics. Interestingly, repeated exposure to QACs recurrently led to a decrease in susceptibility toward ciprofloxacin (CIP), a fluoroquinolone antibiotic, largely used in human medicine. Moreover, these lower levels of susceptibility to CIP remained stable in most Lm strains even after subcultures without biocide selection pressure, suggesting an adaptation involving modifications at the genetic level. Results underlined the ability of Lm to adapt to biocides, especially QACs, and the potential link between this adaptation and the selection of resistance toward critical antibiotics such as ciprofloxacin. These data support a potential role of the extensive use of QACs from “farm to fork” in the selection of biocide and antibiotic resistance in pathogenic bacteria such as Lm. Full article
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Review

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14 pages, 1093 KiB  
Review
Clinical Evidence for the Use of Octenidine Dihydrochloride to Prevent Healthcare-Associated Infections and Decrease Staphylococcus aureus Carriage or Transmission—A Review
by Robin Köck, Luisa Denkel, Andrea T. Feßler, Rudolf Eicker, Alexander Mellmann, Stefan Schwarz, Christine Geffers, Nils-Olaf Hübner and Rasmus Leistner
Pathogens 2023, 12(4), 612; https://doi.org/10.3390/pathogens12040612 - 18 Apr 2023
Cited by 5 | Viewed by 3016
Abstract
Background: The antiseptic agent octenidine dihydrochloride (OCT) is used for skin preparation, for Staphylococcus aureus decolonization, and within bundles for the prevention of catheter-related or surgical site infections (SSIs). Here, we review the evidence for the effects of OCT from clinical studies. Methods: [...] Read more.
Background: The antiseptic agent octenidine dihydrochloride (OCT) is used for skin preparation, for Staphylococcus aureus decolonization, and within bundles for the prevention of catheter-related or surgical site infections (SSIs). Here, we review the evidence for the effects of OCT from clinical studies. Methods: Review of studies published in the Medline, Scopus, and Cochrane databases until August 2022, performed in clinical settings and reporting on effects of OCT on S. aureus carriage/transmission, SSI prevention, and prevention of intensive care unit (ICU)-related or catheter-related bloodstream and insertion site infections. Results: We included 31 articles. The success of S. aureus decolonization with OCT-containing therapies ranged between 6 and 87%. Single studies demonstrated that OCT application led to a reduction in S. aureus infections, acquisition, and carriage. No study compared OCT for skin preparation before surgical interventions to other antiseptics. Weak evidence for the use of OCT for pre-operative washing was found in orthopedic and cardiac surgery, if combined with other topical measures. Mostly, studies did not demonstrate that daily OCT bathing reduced ICU-/catheter-related bloodstream infections with one exception. Conclusions: There is a need to perform studies assessing the clinical use of OCT compared with other antiseptics with respect to its effectiveness to prevent nosocomial infections. Full article
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15 pages, 333 KiB  
Review
Towards a Harmonized Terminology: A Glossary for Biocide Susceptibility Testing
by Szilvia Neuhaus, Andrea T. Feßler, Ralf Dieckmann, Lara Thieme, Mathias W. Pletz, Stefan Schwarz and Sascha Al Dahouk
Pathogens 2022, 11(12), 1455; https://doi.org/10.3390/pathogens11121455 - 1 Dec 2022
Cited by 4 | Viewed by 2002
Abstract
Disinfection is a key strategy to reduce the burden of infections. The contact of bacteria to biocides—the active substances of disinfectants—has been linked to bacterial adaptation and the development of antimicrobial resistance. Currently, there is no scientific consensus on whether the excessive use [...] Read more.
Disinfection is a key strategy to reduce the burden of infections. The contact of bacteria to biocides—the active substances of disinfectants—has been linked to bacterial adaptation and the development of antimicrobial resistance. Currently, there is no scientific consensus on whether the excessive use of biocides contributes to the emergence and spread of multidrug resistant bacteria. The comprehensive analysis of available data remains a challenge because neither uniform test procedures nor standardized interpretive criteria nor harmonized terms are available to describe altered bacterial susceptibility to biocides. In our review, we investigated the variety of criteria and the diversity of terms applied to interpret findings in original studies performing biocide susceptibility testing (BST) of field isolates. An additional analysis of reviews summarizing the knowledge of individual studies on altered biocide susceptibility provided insights into currently available broader concepts for data interpretation. Both approaches pointed out the urgent need for standardization. We, therefore, propose that the well-established and approved concepts for interpretation of antimicrobial susceptibility testing data should serve as a role model to evaluate biocide resistance mechanisms on a single cell level. Furthermore, we emphasize the adaptations necessary to acknowledge the specific needs for the evaluation of BST data. Our approach might help to increase scientific awareness and acceptance. Full article
14 pages, 271 KiB  
Review
Biocidal Resistance in Clinically Relevant Microbial Species: A Major Public Health Risk
by Elaine Meade, Mark Anthony Slattery and Mary Garvey
Pathogens 2021, 10(5), 598; https://doi.org/10.3390/pathogens10050598 - 14 May 2021
Cited by 44 | Viewed by 5743
Abstract
Antimicrobial resistance is one of the greatest dangers to public health of the 21st century, threatening the treatment and prevention of infectious diseases globally. Disinfection, the elimination of microbial species via the application of biocidal chemicals, is essential to control infectious diseases and [...] Read more.
Antimicrobial resistance is one of the greatest dangers to public health of the 21st century, threatening the treatment and prevention of infectious diseases globally. Disinfection, the elimination of microbial species via the application of biocidal chemicals, is essential to control infectious diseases and safeguard animal and human health. In an era of antimicrobial resistance and emerging disease, the effective application of biocidal control measures is vital to protect public health. The COVID-19 pandemic is an example of the increasing demand for effective biocidal solutions to reduce and eliminate disease transmission. However, there is increasing recognition into the relationship between biocide use and the proliferation of Antimicrobial Resistance species, particularly multidrug-resistant pathogens. The One Health approach and WHO action plan to combat AMR require active surveillance and monitoring of AMR species; however, biocidal resistance is often overlooked. ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species) pathogens and numerous fungal species have demonstrated drug and biocidal resistance where increased patient mortality is a risk. Currently, there is a lack of information on the impact of biocide application on environmental habitats and ecosystems. Undoubtedly, the excessive application of disinfectants and AMR will merge to result in secondary disasters relating to soil infertility, loss of biodiversity and destruction of ecosystems. Full article
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